Birds, with a few whacky exceptions (Dumbacher et al. 2008), are not poisonous to eat. I feel like I should cite this paper (Cott & Benson 1969) now too, because I'll probably never get another chance. And, aside from another weird exception (Londoño et al. 2015), birds don't usually look much like anything poisonous. It makes sense then that, unlike butterflies, there's very little Batesian or Müllerian mimicry driving the way birds are colored and patterned. Yet, there are some pretty remarkable instances of what seem to be plumage mimicry in birds. People have talked about these patterns for over 150 years (Wallace 1863), but whether or not these patterns represent socially-mediated convergence, convergent responses to similar environmental pressures, or simply shared evolutionary history has never adequately been resolved (Stresemann 1914, Murray 1976), although recent work has strongly supported the existence of the pattern (Jønsson et al. 2016). Moreover, what the selective pressures might be that would drive such remarkable convergence has been debated (Moynihan 1968, Cody 1969, Barnard 1979, Diamond 1982, Prum 2014). The result has been shockingly little discussion in the literature about what is, if fully corroborated, one of the coolest patterns in birds (me).
[Full disclosure: I proposed doing my dissertation on this subject, but since I didn't have any good related research ideas at the time, that didn't happen]. I'll give you three quick examples. Downy and Hairy Woodpeckers, common backyard denizens and frequent feeder visitors across North America, are not particularly closely related--they are each more closely related to dissimilar looking species--yet they somehow have evolved to look nearly identical to one another in plumage (Weibel & Moore 2005). Ramphastos toucans can be split into two major clades: croakers and yelpers. Across the Americas one can frequently find two sympatric species, one from each clade. And, in approximate parallel across the Americas, they track one another in plumage. White-throated and Channel-billed Toucan in the Amazon, Chestnut-mandibled and Keel-billed in Central America, etc (Weckstein 2005). Then, on either side of the Andes, you have three suboscine genera--Lipaugus, Rhytipterna, and Laniocera--each with a "single" (it's not quite that simple) species on either side. West of the Andes, up into Central America, these are all rufous colored; East of the Andes, these are all gray. Ridgely and Tudor talked about this somewhere in Birds of South America (1994), which was my first exposure to the idea, and Diamond (1982) and Prum (2014) have also talked about it. Anyhow--what? What could possibly be the selective pressures that would drive that? Why would three similar-shaped, somewhat ecologically similar species all "decide" to turn gray in sympatry in the Amazon, and rufous in sympatry in Central America? It certainly doesn't seem like substrate matching. Well, as it turns out, there are at least 7 proposed hypotheses for why this could happen: 1) The larger species would suck to try and kill and eat, and the smaller species mimicked the model to make predators think twice before giving it a go (Wallace 1863). I'm going to add some slight details to this idea, since a paper we're working on now will be able to shed some light on it: the larger (model) species is outside the preferred prey size range of smaller sympatric raptors, and the mimic enjoys reduced predation pressure by looking like the model. 2) All species involved converged on the phenotype to facilitate flocking behavior and thereby reduce predation pressure (Barnard 1979). 3) All species involved converged on the phenotype to facilitate flocking and encourage stereotyped behavioral interactions between flock members (Moynihan 1968). 4) All species involved converged on the phenotype to facilitate interspecific territorial interactions (Cody 1969). 5) The larger species converged on the model (the smaller species) so as to fool predators into believing it to not be a worthwhile target (the skin and bones hypothesis). I don't know a citation for this idea, but it's out there. 6) The smaller species converged on the model so as to confuse the model and experience reduced aggression from the model (Diamond 1982, Prum & Samuelson 2012). 7) The smaller species converged on the model so as to confuse third parties and hold a more dominant position around contested resources than it otherwise would (Wallace 1863, Diamond 1982). NB: in our recent paper (below), we attributed this last idea solely to Wallace, a view likewise stated by Prum and Samuelson (2012) and Prum (2014). However, I have recently more carefully read those original Wallace papers, and Jønsson et al. (2016) and Diamond (1982) are more accurate in stating Wallace's idea had to do with hypothesis 1, above. To be fair, Wallace was sort of agnostic about the precise driver, and his brief passages could be interpreted as giving rise to hypothesis 7, but I now think hypothesis 7 is best attributed to Diamond (1982). I guess the moral of the story is that arguing 155 years later over which evolutionary driver Wallace was invoking four years after the publication of the Origin of the Species is a fool's errand. Wallace seems like a fine choice. So what is the evidence for and against each of these hypotheses? 1) Sorry, but you'll have to keep your eyes out for our third installment from Project FeederWatch, which looks at the predation data that participants have submitted. Otherwise, no experimental evidence in birds that I know of. Hypothesis 1 remains standing. 2) Seems unlikely to me that species would converge on visually obvious phenotypes when they could just as well blend into the background, but I guess that doesn't kill this hypothesis entirely. To invoke sexual selection as as a driver of bold plumages, and then suggest this group-level selection somehow drives near perfect plumage convergence seems fraught, but we'll leave it as a hypothesis someone with a lot of time on their hands might want to look into. 3) Community selection? Not a lot of support for that. Here are Moynihan's 5 predictions from his paper. A) Related species which are sympatric will usually be more similar in overall appearance, on the average, than equally closely related species of similar habits which are allopatric. B) The closer and more frequent are the contacts between individuals of sym- patric species, the closer will be the resem- blances between them. C) Resemblances among sympatric spe- cies should be positively correlated with age of sympatry. Species which have been sympatric for a long time (without diverg- ing ecologically to such an extent as to prevent contacts between individuals of the different species) will be more similar in overall appearance, on the average, than comparable species which have been sym- patric for a short time. D) "Old" faunas (which have evolved for some appreciable length of time with- out being invaded by species from other areas) should include larger numbers of similar-appearing species than otherwise comparable "young" faunas. E) The strength and extent of resem- blances among sympatric species should be positively correlated with the number of species involved. The more species overlap and come into contact with one another frequently, the more likely it is that they will evolve convergent resem- blances for social mimicry. (This, of course, is one of the reasons why social mimicry is more conspicuous, and pre- sumably more common, in tropical conti- nental areas than in other regions.) There is strong evidence against most of these ideas, e.g. (Martin et al. 2015, Pigot & Tobias 2013). So, I'd say we can scratch hypothesis 3 off the list. 4) Again, there is not much empirical evidence out there showing that natural selection operates at these sorts of community levels. Species that hold mutually interspecific territories appear fully capable of distinguishing one another based on numerous characteristics such as vocalizations--they don't need to look like one another to make those distinctions. The idea here is that looking similar means that interactions between individuals are "definite". We look like each other so we know we're fighting here, no beating around the trunk trying to figure out if we want to fight at all. Many species that are agonistic towards one another over large portions of their range look nothing alike, and many species that look alike do not seem to hold interspecific territories. Given that, plus all the other selective pressures on plumages, I find this hypothesis really unlikely. Let's scratch it off the list. 5) Maybe, but unlikely in my opinion. We should hopefully be able to indirectly address it in our forthcoming FeederWatch predation paper. A prediction would be that both species would suffer low predation risk. I'm not saying it's impossible, but it would be much like a monarch mimicking a tasty skipper butterfly. 6) I see Hairy Woodpeckers occasionally displace Downy Woodpeckers in the forest in natural settings. Kilham (1972) saw a Campephilus woodpecker displace its mimic Dryocopus in Panama. Most birds seem able to recognize specific individuals of their own species. I have always found the idea that the purported model species somehow chooses not to attack the smaller mimic, when it would likely attack an unknown individual of its own species, difficult to believe. Fortunately, we don't have to rely on my feelings for whether to strike this hypothesis from the list. In a recent paper (Leigton et al. 2018) we tested the idea, and found strong evidence against it. Instead of experiencing reduced aggression, Downy Woodpeckers (the purported mimics) receive ample aggression from Hairy Woodpeckers--much more than would be expected based on the species' relative abundances. There is a slight caveat here: our study took place around feeders, which could be argued are artificial boxing rings. Yet, the evidence came down so hard against this idea, I'm striking it from my own list of reasonable hypotheses. Show me some experimental evidence and I'll change my tune. Instead of supporting this hypothesis, we found some support for the fact that... 7) It seems that Downy Woodpeckers hold slightly higher positions in the dominance hierarchy than would be expected based on their body mass and phylogenetic position. What do I mean by that? Well, we recently showed that woodpeckers tend to be dominant in general, and that body mass does a good job of predicting species' dominance ranks (Miller et al. 2016). So, even after accounting for that boost in dominance, Downy Woodpeckers are more dominant than expected based on their body mass. Indeed, they are predicted to be less dominant than House Sparrows, Song Sparrows, White-throated Sparrows, Yellow-rumped Warblers, and maybe even White-breasted Nuthatches (Leighton et al. 2018). So, is the fact that they look like Hairy Woodpeckers the thing that gives Downy the boost in the fight club rankings? We think it's likely, but the jury's still out. Literature cited: Barnard, C. J. (1979). Predation and the evolution of social mimicry in birds. The American Naturalist, 113(4), 613-618. Cody, M. L. (1969). Convergent characteristics in sympatric species: a possible relation to interspecific competition and aggression. Condor, 71(3), 223-239. Cott, H. B., & Benson, C. W. (1969). The palatability of birds, mainly based upon observations of a tasting panel in Zambia. Ostrich, 40(S1), 357-384. Diamond, J. M. (1982). Mimicry of friarbirds by orioles. The Auk, 99, 187-196. Dumbacher, J. P., Deiner, K., Thompson, L., & Fleischer, R. C. (2008). Phylogeny of the avian genus Pitohui and the evolution of toxicity in birds. Molecular Phylogenetics and Evolution, 49(3), 774-781. Jønsson, K. A., Delhey, K., Sangster, G., Ericson, P. G., & Irestedt, M. (2016). The evolution of mimicry of friarbirds by orioles (Aves: Passeriformes) in Australo-Pacific archipelagos. Proceedings of the Royal Society B: Biological Sciences, 283, 20160409. http://dx.doi.org/10.1098/rspb.2016.0409 Kilham, L. (1972). Habits of the Crimson-crested Woodpecker in Panama. The Wilson Bulletin, 84(1), 28-47. Leighton, G. M., Lees, A. C., & Miller, E. T. (2018). The Hairy-Downy game revisited: an empirical test of the Interspecific Social Dominance Mimicry Hypothesis. Animal Behaviour, 137, 141-148. https://doi.org/10.1016/j.anbehav.2018.01.012 Londoño, G. A., García, D. A., & Martínez, M. A. S. (2015). Morphological and behavioral evidence of Batesian mimicry in nestlings of a lowland Amazonian bird. The American Naturalist, 185(1), 135-141. Martin, P. R., Montgomerie, R., & Lougheed, S. C. (2015). Color patterns of closely related bird species are more divergent at intermediate levels of breeding-range sympatry. The American Naturalist, 185(4), 443-451. https://doi.org/10.1086/680206 Miller, E. T., Bonter, D. N., Eldermire, C., Freeman, B. G., Greig, E. I., Harmon, L. J., … Hochachka, W. M. (2017). Fighting over food unites the birds of North America in a continental dominance hierarchy. Behavioral Ecology, Online Early. https://doi.org/10.1093/beheco/arx108 Moynihan, M. (1968). Social mimicry; character convergence versus character displacement. Evolution, 22(2), 315-331. Murray, B. G. (1976). A critique of interspecific territoriality and character convergence. The Condor, 78(4), 518-525. Pigot, A. L., & Tobias, J. A. (2013). Species interactions constrain geographic range expansion over evolutionary time. Ecology Letters, 16(3), 330-338. https://doi.org/10.1111/ele.12043 Prum, R. O. (2014). Interspecific social dominance mimicry in birds. Zoological Journal of the Linnean Society, 172(4), 910-941. Prum, R. O., & Samuelson, L. (2012). The Hairy-Downy Game: A model of interspecific social dominance mimicry. Journal of Theoretical Biology, 313, 42-60. Prum, R. O., & Samuelson, L. (2016). Mimicry cycles, traps, and chains: the coevolution of toucan and kiskadee mimicry. The American Naturalist, 187(6), 753-764. Ridgely, R. S., & Tudor, G. (1994). Birds of South America Volume II, The Suboscine Passerines: Ovenbirds and Woodcreepers, Antbirds, Gnateaters, and Tapaculos, Tyrant Flycatchers, Manakins and Cotingas. Austin: The University of Texas. Wallace, A. R. (1863). List of birds collected in the island of Bouru (one of the Moluccas), with descriptions of new species. Proceedings of the Zoological Society of London, 1863, 18-28. Weckstein, J. D. (2005). Molecular phylogenetics of the Ramphastos toucans: implications for the evolution of morphology, vocalizations, and coloration. The Auk, 122(4), 1191-1209. Weibel, A. C., & Moore, W. S. (2005). Plumage convergence in Picoides woodpeckers based on a molecular phylogeny, with emphasis on convergence in downy and hairy woodpeckers. The Condor, 107(4), 797-809.
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